Isogenic bacterial populations can display probabilistic cell-to-cell variation
in response to challenges. This phenotypic heterogeneity can affect virulence
in animals, but its impact on plant pathogens is unknown. Previously, we
showed that expression of the type III secretion system (T3SS) of the plant
pathogen Pseudomonas syringae displays phenotypic variation in planta.
Here we use flow cytometry and microscopy to investigate single-cell flagellar
expression in relation to T3SS expression, showing that both systems
undergo phenotypic heterogeneity in vitro in apoplast-mimicking medium
and within apoplastic microcolonies throughout colonization of Phaseolus
vulgaris. Stochastic, spatial and time factors shape the dynamics of a
phenotypically diverse pathogen population that displays division of labour
during colonization: effectors produced by T3SS-expressing bacteria act as
‘common goods’ to suppress immunity, allowing motile flagella-expressing
bacteria to increase and leave infected tissue before necrosis. These
results showcase the mechanisms of bacterial specialization during plant
colonization in an environmentally and agriculturally relevant system.